Abstract
Plant cells utilize various sugars as carbon sources for growth, respiration and biosynthesis of cellular components. Suspension-cultured cells of azuki bean (Vigna angularis) proliferated actively in liquid growth medium containing 1% (w/v) sucrose, glucose, fructose, arabinose or xylose, but did not proliferate in medium containing galactose or mannose. These two latter sugars thus appeared distinct from other sugars used as growth substrates. Galactose strongly inhibited cell growth even in the presence of sucrose but mannose did not, suggesting a substantial difference in their effects on cell metabolism. Analysis of intracellular soluble-sugar fractions revealed that galactose, but not mannose, caused a conspicuous decrease in the cellular level of sucrose with no apparent effects on the levels of glucose or fructose. Such a galactose-specific decrease in sucrose levels also occurred in cells that had been cultured together with glucose in place of sucrose, suggesting that galactose inhibits the biosynthesis, rather than uptake, of sucrose in the cells. By contrast, mannose seemed to be metabolically inert in the presence of sucrose. From these results, we conclude that sucrose metabolism is important for the heterotrophic growth of cells in plant suspension-cultures.
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Brouquisse R, Evrard A, Rolin D (2001) Regulation of protein degradation and protease expression by mannose in maize root tip. Pi sequestration by mannose may hinder the study of its signaling properties. Plant Physiol 125:1485–1498
Carpita NC, Brown RA, Weller KM (1982) Uptake and metabolic fate of glucose, arabinose, and xylose by Zea mays coleoptiles in relation to cell wall synthesis. Plant Physiol 69:1173–1180
Delmer DP, Amor Y (1995) Cellulose biosynthesis. Plant Cell 7:987–1000
Dodds JH, Roberts LW (1985) Cell suspension cultures. In: Experiments in plant tissue culture, 2nd edn. Cambridge University Press, New York, pp 104–112
Elling L, Grothus M, Kula MR (1993) Investigation of sucrose synthase from rice for the synthesis of various nucleotide sugars and saccharides. Glycobiology 3:349–355
Goldworthy A, Street HE (1965) The carbohydrate nutrition of tomato roots VIII. The mechanism of the inhibition by d-mannose of respiration of excised roots. Ann Bot 29:45–58
Göring H, Gerlach I (1966) Wachstum kurzfristig isolierter pflanzlicher Gewebe in Abhangigkeit von der exogenen Kohlenstoffquelle. Z Pflanzenphysiol Bd 55:429–444
Göring H, Reckin E (1968) Galactose-1-phosphate as inhibitor of polysaccharide synthesis in higher plants. Naturwissenschaften 55:40–41
Gross KC, Pharr DM, Locy RD (1981) Growth of callus initiated from cucumber hypocotyls on galactose and galactose-containing oligosaccharides. Plant Sci Lett 20:333–341
Herold A, Lewis DH (1977) Mannose and green plants: occurrence, physiology and metabolism, and use as a tool to study the role of orthophosphate. New Phytol 79:1–40
Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438
Inouhe M, Yamamoto R, Masuda Y (1986) Inhibition of IAA-induced cell elongation in Avena coleoptile segments by galactose: its effect on UDP-glucose formation. Physiol Planta 66:370–376
Inouhe M, Yamamoto R, Masuda Y (1987) Effects of indoleacetic acid and galactose on the UTP level and UDP-glucose formation in Avena coleoptile and Vigna epicotyl segments. Physiol Planta 69:579–585
Inouhe M, Yamamoto R (1991) Effects of 2-deoxygalactose on auxin-induced growth and levels of UDP-sugars in higher plants. Plant Cell Physiol 32:433–438
Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540
Koch KE (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246
Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372
Maretzki A, Thom M (1978) Characteristics of galactose-adapted sugarcane cell line grown in suspension culture. Plant Physiol 61:544–548
Maynard JW, Lucas WJ (1982b) Sucrose and glucose uptake into Beta vulgaris leaf tissues. Plant Physiol 70:1436–1443
Miyamoto K, Kamisaka S (1990) Effect of gibberellic acid on epicotyl growth and carbohydrate distribution in derooted Pisum sativum cuttings with or without cotyledons. Physiol Planta 80:357–364
Miyamoto K, Ueda J, Kamisaka S (1992) Sugar accumulation in growing subhooks of etiolated Pisum sativum seedlings-Stimulation of sugar exdation and invertase activity in epicotyls by gibberellic acid. Physiol Planta 84:106–112
Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 33:299–319
Morgan DR, Street HE (1959) The carbohydrate nutrition of tomato roots. VII. Sugars, sugar phosphates and sugar alcohols as respiratory substrates for excised roots. Ann Bot 23:89–105
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Planta 15:473–493
Nygaard P (1971) Studies on the germination of pine pollen (Pinus mugo) in vitro: III. Inhibition by d-mannose and deoxyhexoses. Physiol Planta 24:130–136
Pego JV, Weisbeek PJ, Smeekens CM (1999) Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiol 119:1017–1023
Riesmeier JW, Willmitzer L, Frommer WB (1994) Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J 13:1–7
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709
Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54:525–531
Smeekens S, Rook F (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol 115:7–13
Stenlid G (1954) Toxic effects of d-mannose, 2-deoxy-d-glucose and d-glucosamine upon respiration and ion absorption in wheat roots. Physiol Plant 7:73–81
Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407
Verma DC, Dougall DK (1977) Influence of carbohydrates on quantitative aspects of growth and embryo formation in wild carrot suspension cultures. Plant Physiol 59:81–85
Verma DC, Dougall DK (1979) myo-Inositol biosynthesis and galactose utilization by wild carrot (Daucus carota L. var. Carota) suspension cultures. Ann Bot 43:259–269
Yamamoto R, Inouhe M, Masuda Y (1988) Galactose inhibition of auxin-induced growth of mono-and dicotyledonous plants. Plant Physiol 86:1223–1227
Acknowledgments
We wish to thank to Hiroki Nakahara, Toshihisa Kamichi, Kazuhiro Yamamoto and Satoshi Nozaki for their contribution in the present study.
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Kato, A., Tohoyama, H., Joho, M. et al. Different effects of galactose and mannose on cell proliferation and intracellular soluble sugar levels in Vigna angularis suspension cultures. J Plant Res 120, 713–719 (2007). https://doi.org/10.1007/s10265-007-0117-9
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DOI: https://doi.org/10.1007/s10265-007-0117-9